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Domestication Syndrome” in Light of Genomic Data Вавиловский журнал генетики и селекции. 2017;21(4):435­442 Эволюционная генетика DOI 10.18699/VJ17.262 ОБЗОР / REVIEW Revisiting two hypotheses on the “domestication syndrome” in light of genomic data A.S. Wilkins Institute of Theoretical Biology, Humboldt Universität zu Berlin, Berlin, Germany Domesticated mammals of many different species share a set of «Синдром одомашнивания» physical and physiological traits that are not displayed by any of their wild progenitors. This suite of traits, now termed the “domestication в свете геномных данных syndrome” (DS), has been a puzzle since Charles Darwin discovered it. Two general explanations of its basis have been proposed, which in А.С. Уилкинс principle, could also apply to other vertebrates, such as fish and birds, whose domesticated varieties show some of its elements. The two Институт теоретической биологии Берлинского ideas are termed here, respectively, the thyroid hormone hypothesis университета им. Гумбольдта, Берлин, Германия or the THH, and the neural crest cell hypothesis, the NCCH. The two ideas make distinctly different genetic predictions. Here, the current relevant evidence from genomics is evaluated and it is concluded that Доместицированные млекопитающие разных видов the NCCH has more support. Nevertheless, one set of observations, имеют общий набор физических и физиологических from chickens, suggest a potentially important role of altered thyroid признаков, которых не было у их диких предков. metabolism in domestication. In addition, recent studies indicate the Совокупность этих признаков, называемая «синдро­ possibility of additional genetic factors in domestication, affecting мом одомашнивания», остается загадкой со времен tameness and sociality, that may go beyond either hypothesis. The Чарльза Дарвина, открывшего этот феномен. В на­ tasks that lie ahead to fully ascertain the genetic bases of the “domes­ стоящее время существуют две общие гипотезы, tication syndrome” and the behaviors that characterize mammalian объясняющие это явление, которые отчасти при­ domestication are discussed briefly. менимы и к другим позвоночным, например рыбам и птицам. Одну из этих гипотез мы называем гипоте­ Key words: animal domestication; “domestication syndrome”; Charles зой тиреоидных гормонов (THH), а другую – гипо­ Darwin; comparative genomics; neoteny; neural crest cells; thyroid тезой клеток нервного гребня (NCCH). Каждая из metabolism. гипотез приводит к совершенно разным выводам на уровне генетики. Основываясь на анализе по­ следних данных геномных исследований, имеющих отношение к обсуждаемому вопросу, мы пришли к выводу, что более обоснованной выглядит гипотеза NCCH. Тем не менее ряд наблюдений, сделанных на курах, указывает на потенциально важную роль из­ мененного метаболизма тиреоидных гормонов для процесса одомашнивания. Кроме того, недав ние исследования указывают на возможность существо­ вания дополнительных факторов одомашнивания, оказывающих влияние на приручаемость и социаль-­ ность и не учитываемых ни одной из рассматрива­ емых гипотез. Кратко обсуждаются задачи, направ­ ленные на выявление генетических основ «синдро­ ма одомашнивания» и особенностей поведения, специфичных для процесса одомашнивания млеко­ питающих. Ключевые слова: одомашнивание животных; «син­ дром одомашнивания»; Чарльз Дарвин; сравни­ тельная геномика; неотения; клетки нервного КАК ЦИТИРОВАТЬ ЭТУ СТАТЬЮ: гребня; метаболизм тиреоидных гормонов. Уилкинс А.С. «Синдром одомашнивания» в свете геномных данных. Вавиловский журнал генетики и селекции. 2017;21(4):435­442. DOI 10.18699/VJ17.262 HOW TO CITE THIS ARTICLE: Wilkins A.S. Revisiting two hypotheses on the “domestication syndrome” in light of genomic data. Vavilovskii Zhurnal Genetiki i Selektsii = Vavilov Jour­ nal of Genetics and Breeding. 2017;21(4):435­442. DOI 10.18699/VJ17.262 УДК 591.612:577.175.44 Поступила в редакцию 09.03.2017 г. Принята к публикации 10.05.2017 г. © АВТОР, 2017 e­mail: [email protected] he domestication of animals and, in particular, that of it): Charles Darwin. He had been trying to develop a theory various mammalian species, was crucial for the develop- of the nature of heredity since at least the early 1850s and in Tment of human civilizations (Diamond, 1999; Larson et 1868 published his monumental work on heredity, Variation al., 2014; Francis, 2015). Involving more than 20 mammalian of Animals and Plants under Domestication (Darwin, 1868). species, and a few bird and fish species, animal domestica- Darwin was writing decades before there was an experimental tion commenced in different places on different continents science of genetics, or even any kind of theoretical framework at different times but took place primarily during the past for understanding biological inheritance, and he had to rely 11–10,000 years, following the rise of agriculture (see Larson on the work of animal and plant breeders for the data he col- et al., 2014, Fig. 1). (The dog is one species, however, whose lected. In the course of compiling all the information for his initial domestication took place considerably earlier, and per- monumental work on heredity, he noticed that domesticated haps twice, independently, probably more than 15,000 years breeds, regardless of species, tended to share a common set of ago (Frantz et al., 2016).) visible traits, most of those listed above. (The physiological Given the historical importance of the domestication of traits of the DS were discovered much later, however.) mammals, it is of great interest to understand both its historical There are two particularly puzzling aspects of the condition. roots and its biological basis. Although there are many specific First is the variety of the different traits of the DS, which share questions about the histories of the different domestication little immediate obvious connection with each other. Second is events, the places and approximate dates for many species are the fact that the initial selection in each instance of domestica- increasingly well known (Larson et al., 2014; Francis, 2015). tion was almost certainly for tameness, permitting humans to The biology underlying domestication, however, presents a get close to the animals involved. (This pertains even to the major puzzle. Although the domestication of each species must evolution of dogs from wolves, where there may not have been have involved direct or indirect selection for docility (lack deliberate taming by humans but a self-selection of individual of fear) and tameness (ability to be handled by humans), the animals who neither attacked nor fled from people around domesticated breeds of the different mammalian species all human settlements.) The other traits were apparently dragged share a distinctive suite of physical and physiological traits, along as consequences of the initial selection, through poorly not seen in their wild progenitors. The suite of traits is neither understood connections. This phenomenon, in which selection universal amongst species nor amongst all breeds of a given for one trait brings in train one or more additional, unexpected species (Sanchez-Villagra et al., 2016). Nevertheless, it is traits, Darwin termed “unconscious selection” though perhaps sufficiently generic to be seen as a signature feature of mam- “unintended co-selection” might be more apt. malian domestication. The relationship of these traits to the Darwin’s own explanation of the phenomenon was neither initial selected traits of docility and tameness, however, is not totally self-consistent nor complete. He wanted to ascribe these readily apparent. The particular secondary morphological and changes to the gentler “conditions of living” provided by the physiological traits that mark the domesticated state include: anthropogenic environment but he also realized that in many floppy ears, smaller jaws, smaller teeth, pigmentation changes cases, the characteristics were or had become heredity, hence in the coats (toward white and brown spots), reductions in not solely a function of the anthropogenic environment. Fur- adrenocortical hormone titers, increased frequency of estrus thermore, he could not explain why the particular traits seen, cycles, reduction in brain size, and alterations in concentration and not others, were the ones that appeared in association with of several brain neurotransmitters. (For a comprehensive tally the domesticated state. It is, of course, not puzzling that he of which domestication-specific traits appear in the different himself could not answer the question in the 19th century, even mammalian species that have been domesticated, see Figure 1 approximately, given the general ignorance of Mendel’s work, of Sanchez-Villagra et al., 2016.) which would eventually provide the foundations of modern This condition has been dubbed the “domestication syn- genetics. What is perhaps more surprising in retrospect is that drome”, abbreviated here as the DS. The term itself appears 20th century genetics also failed to solve the problem. Some to have been first used in connection with a parallel set of heroic and important large efforts were made, however, and observed commonalities amongst domesticated plants (Ham- a significant start was made with the work of the pioneering mer, 1984) but was later applied to animals (Larson et al., Soviet geneticist Dmitry Belyaev and his colleagues from the 2014; Wilkins et al., 2014). (Some authors, however, prefer early 1960s onwards (Belyaev, 1974, 1979; reviewed in Trut the term “domesticated phenotype” to avoid the implication et
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